Intrauterine programming of bone. Part 1: Alteration of the osteogenic environment

Osteoporosis International

Volumn 19, Issue 2, 2008, Pages 147-156

  Lanham, S A ^a,b   Roberts, C ^a   Cooper, C ^a   Oreffo, R O C ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b SOUTHAMPTON GENERAL HOSPITAL   (United Kingdom)

Author keywords

Bone marrow; In utero; Maternal; Osteogenic programming

Indexed keywords

25 HYDROXYVITAMIN D; ALKALINE PHOSPHATASE; OSTEOCALCIN; SOMATOMEDIN C;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; MALE; NONHUMAN; OSTEOPOROSIS; PREGNANCY; PRIORITY JOURNAL; PROGENY; PROTEIN DIET; RAT;

AGING; ALKALINE PHOSPHATASE; ANIMALS; BIRTH WEIGHT; BONE AND BONES; BONE MARROW CELLS; CALCIFEDIOL; CELLS, CULTURED; DIET, PROTEIN-RESTRICTED; FEMALE; INSULIN-LIKE GROWTH FACTOR I; LITTER SIZE; MALE; OSTEOCALCIN; OSTEOGENESIS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PRENATAL NUTRITION PHYSIOLOGY; RATS; RATS, WISTAR; WEIGHT GAIN;

EID: 37749013339     PISSN: 0937941X     EISSN: 14332965     Source Type: Journal    
DOI: 10.1007/s00198-007-0443-8     Document Type: Article

References (40)

1. NIH Consensus Development Panel on Osteoporosis Prevention DaT (2001) Osteoporosis Prevention, Diagnosis, and Therapy. JAMA 285:785-795
2. Ralston SH (1998) Do genetic markers aid in risk assessment? Osteoporos Int 8(Suppl 1):S37-S42
3. Cooper C, Cawley M, Bhalla A et al (1995) Childhood growth, physical activity, and peak bone mass in women. J Bone Miner Res 10:940-947
4. Cooper C, Fall C, Egger P et al (1997) Growth in infancy and bone mass in later life. Ann Rheum Dis 56:17-21
5. Cooper C, Javaid MK, Taylor P et al (2002) The fetal origins of osteoporotic fracture. Calcif Tissue Int 70:391-394
6. Fall C, Hindmarsh P, Dennison E et al (1998) Programming of growth hormone secretion and bone mineral density in elderly men: a hypothesis. J Clin Endocrinol Metab 83:135-139
7. Godfrey KM, Barker DJ (2000) Fetal nutrition and adult disease. Am J Clin Nutr 71:1344S-1352S
8. Barker DJ (1992) The fetal origins of diseases of old age. Eur J Clin Nutr 46 Suppl 3:S3-S9
9. Cooper C, Walker-Bone K, Arden N et al (2000) Novel insights into the pathogenesis of osteoporosis: the role of intrauterine programming. Rheumatology (Oxford) 39:1312-1315
10. Langley-Evans SC, Welham SJ, Jackson AA (1999) Fetal exposure to a maternal low protein diet impairs nephrogenesis and promotes hypertension in the rat. Life Sci 64:965-974
11. Langley-Evans SC (1999) Fetal origins of adult disease. Br J Nutr 81:5-6
12. Aihie S, Dunn R, Langley-Evans SC et al (2001) Prenatal exposure to a maternal low protein diet shortens life span in rats. Gerontology 47:9-14
13. Roach H, Langley-Evans SC, Cooper C (1999) Protein deficiency during pregnancy affects skeletal development in the offspring. J Bone Miner Res 14(suppl 1):S394
14. Mehta G, Roach HI, Langley-Evans S et al (2002) Intrauterine exposure to a maternal low protein diet reduces adult bone mass and alters growth plate morphology in rats. Calcif Tissue Int 71:493-98
15. Langley-Evans SC, Welham SJ, Sherman RC et al (1996) Weanling rats exposed to maternal low-protein diets during discrete periods of gestation exhibit differing severity of hypertension. Clin Sci (Lond) 91:607-615
16. Ammann P, Bourrin S, Bonjour JP et al (2000) Protein undernutrition- induced bone loss is associated with decreased IGF-I levels and estrogen deficiency. J Bone Miner Res 15:683-690
17. Bourrin S, Toromanoff A, Ammann P et al (2000) Dietary protein deficiency induces osteoporosis in aged male rats. J Bone Miner Res 15:1555-1563
18. Bourrin S, Ammann P, Bonjour JP et al (2000) Dietary protein restriction lowers plasma insulin-like growth factor I (IGF-I), impairs cortical bone formation, and induces osteoblastic resistance to IGF-I in adult female rats. Endocrinology 141:3149-3155
19. Oreffo RO, Lashbrooke B, Roach HI et al (2003) Maternal protein deficiency affects mesenchymal stem cell activity in the developing offspring. Bone 33:100-107
20. Oreffo RO, Kusec V, Romberg S et al (1999) Human bone marrow osteoprogenitors express estrogen receptor-alpha and bone morphogenetic proteins 2 and 4 mRNA during osteoblastic differentiation. J Cell Biochem 75:382-392
21. Oreffo R, Cooper C, Mason C et al (2005) Mesenchymal Stem cells: Lineage, plasticity and skeletal therapeutic potential. Stem Cell Rev 1:169-178
22. Langley-Evans SC, Nwagwu M (1998) Impaired growth and increased glucocorticoid-sensitive enzyme activities in tissues of rat fetuses exposed to maternal low protein diets. Life Sci 63:605-615
23. Gluckman PD, Hanson MA (2004) Living with the past: evolution, development, and patterns of disease. Science 305:1733-1736
24. Bateson P, Barker D, Clutton-Brock T et al (2004) Developmental plasticity and human health. Nature 430:419-421
25. Muaku SM, Thissen JP, Gerard G et al (1997) Postnatal catch-up growth induced by growth hormone and insulin-like growth factor-I in rats with intrauterine growth retardation caused by maternal protein malnutrition. Pediatr Res 42:370-377
26. Reichling TD, German RZ (2000) Bones, Muscles and Visceral Organs of Protein-Malnourished Rats (Rattus norvegicus) Grow More Slowly but for Longer Durations to Reach Normal Final Size. J Nutr 130:2326-2332
27. Miller JP, German RZ (1999) Protein Malnutrition Affects the Growth Trajectories of the Craniofacial Skeleton in Rats. J Nutr 129:2061-2069
28. Brown JP, Delmas PD, Malaval L et al (1984) Serum bone Gla-protein: a specific marker for bone formation in postmenopausal osteoporosis. Lancet 1:1091-1093
29. Siebler T, Robson H, Shalet SM et al (2001) Glucocorticoids, thyroid hormone and growth hormone interactions: implications for the growth plate. Horm Res 56 Suppl 1:7-12
30. Hunziker EB, Schenk RK (1989) Physiological mechanisms adopted by chondrocytes in regulating longitudinal bone growth in rats. J Physiol (Lond) 414:55-71
31. Kember NF (1973) Aspects of the maturation process in growth cartilage in the rat tibia. Clin Orthop Relat Res 95:288-294
32. Yakar S, Rosen CJ, Beamer WG et al (2002) Circulating levels of IGF-1 directly regulate bone growth and density. J Clin Invest 110:771-781
33. Yakar S, Liu JL, Stannard B et al (1999) Normal growth and development in the absence of hepatic insulin-like growth factor I. PNAS 96:7324-7329
34. Ringe JD (1998) Vitamin D deficiency and osteopathies. Osteoporos Int 8:S35-S39
35. Ozaki T, Nishina H, Hanson MA et al (2001) Dietary restriction in pregnant rats causes gender-related hypertension and vascular dysfunction in offspring. J Physiol (Lond) 530:141-152
36. Ozanne SE, Smith GD, Tikerpae J et al (1996) Altered regulation of hepatic glucose output in the male offspring of protein-malnourished rat dams. Am J Physiol Endocrinol Metab 270:E559-E564
37. Lind L, Hanni A, Lithell H et al (1995) Vitamin d is related to blood pressure and other cardiovascular risk factors in middle-aged men. Am J Hypertens 8:894-901
38. McMullen S, Langley-Evans SC (2005) Maternal low-protein diet in rat pregnancy programs blood pressure through sex-specific mechanisms. Am J Physiol Regul Integr Comp Physiol 288:R85-R90
39. McMullen S, Langley-Evans SC (2005) Sex-Specific Effects of Prenatal Low-Protein and Carbenoxolone Exposure on Renal Angiotensin Receptor Expression in Rats. Hypertension 46:1374-1380
40. Langley-Evans SC, Sculley DV (2005) Programming of hepatic antioxidant capacity and oxidative injury in the ageing rat. Mech Ageing Dev 126:804-812